220 Opinion TRENDS in Ecology and Evolution
5 May 2003
Phylogenetic comparative methods
and the geography of speciation
Jonathan B. Losos and Richard E. Glor
Department of Biology, Campus Box 1137, Washington University, St Louis, MO 63130-4899, USA
The geography of speciation has long been contentious.
In recent years, phylogenetic approaches have been
proposed to determine the geographical mode of speci-
ation. If reliable, these methods not only provide a
means of settling the debate about the geography of
speciation, but also indicate that sympatric speciation
is surprisingly common and that peripatric speciation is
relatively rare. Similar to any phylogenetic inference,
reconstructions of speciation mode are only useful if
the underlying assumptions of the method are met. In
this case, the key assumption is that the geographical
range of both extant and ancestral species at the time
of speciation can be inferred from present-day distri-
butions. We discuss whether, and under what circum-
stances, such assumptions could be met. We conclude
that interspecific phylogenies are unable to test alterna-
tive hypotheses concerning the geography of speciation
rigorously because of the lability of geographical ranges
and the lack of correlation between the role of adaptive
processes and geographical mode of speciation.
In spite of half a century of research, resolution of the
controversies concerning the manner in which SPECIATION
(see Glossary) occurs does not appear to be imminent [1].
Given the great success of phylogenetic approaches over
the past 15 years in addressing a wide variety of
evolutionary questions (e.g. [2– 6]), attempts to apply
these methods to the study of speciation are not surprising
(reviewed in [7]).
Spurred by Lynch’s influential paper [8], recent studies
have attempted to use interspecific phylogenetic com-
parative methods to address one of the most contentious
issues in speciation: the geographical mode of speciation
[2,9 – 24]. The results of such studies have attracted
considerable attention, both for their promise of resolving
long-standing questions and for their unexpected findings,
such as the suggestions that PERIPATRIC SPECIATION is
relatively rare and that SYMPATRIC SPECIATION is surpris-
ingly common [2,8,11,14,19]. If reliable, these methods at
last provide an effective approach toward settling disputes
about the frequencies of different geographical modes of
speciation. However, if the assumptions of these methods
are not met, the resulting conclusions might not be
reliable. Here, we assess the extent to which these
assumptions are realistic and evaluate the contribution
Corresponding author: Jonathan B. Losos (losos@biology.wustl.edu).
http://tree.trends.com 0169-5347/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0169-5347(03)00037-5
Vol.18 No.
that such phylogenetic approaches can make to the study
of the geography of speciation.
Phylogenetic approaches and the geography of
speciation
Methods and assumptions
Most interspecific phylogenetic approaches to the geo-
graphy of speciation work by examining the distribution of
sister taxa: for example, if they are sympatric, then
speciation is inferred to have been sympatric and if they
are allopatric, speciation is inferred to have been allopatric
(Fig. 1). For extant taxa, this approach leads to the
comparison of sister species; for deeper nodes in a
phylogeny, the procedure becomes more complicated
because the geographical distribution of ancestral taxa
must first be inferred (Box 1).
The Achilles heel of this approach is that it requires the
reconstruction of the geographical distribution of species
at the time of speciation. The obvious problem with this
approach is that the current distribution of a species is
not necessarily a reliable indicator of the historical
geographical range of the same species (K.A. Crandall,
PhD thesis, Washington University, 1993, [8,9,14,24,25]).
One need only consider the alteration of the ranges of
species that occurred during and after the Quaternary ‘Ice
Ages’ to recognize how radically ranges have shifted in
recent evolutionary history, not only in glaciated areas
[26 –28], but also in tropical forests and oceans [29 – 31].
Three lines of evidence indicate that the geographical
range of species can, and often does, change substantially
over short periods of time because of climate change,
colonization of new areas, extinction of competitors, and a
host of other reasons. First, the fossil record documents the
Glossary
Allopatric speciation: speciation resulting from divergent evolution of
populations that are geographically isolated from each other.
Parapatric speciation: speciation resulting from divergent evolution of
populations that are geographically adjacent to each other.
Peripatric speciation: a subset of allopatric speciation in which a peripherally
isolated population diverges to become a new species.
Peripheral isolates: a geographically isolated population on the periphery of a
species’ range.
Speciation: divergent evolution resulting in two species from an initial
ancestral species.
Sympatric speciation: speciation occurring within a single geographical area.
Vicariant speciation: a subset of allopatric speciation in which two populations
become isolated by the fragmentation of an initially continuous range into two
or more allopatric populations, each of which is substantial in size (i.e. neither
is a peripheral isolate).
 Opinion TRENDS in Ecology and Evolution
Fig. 1. Testing hypotheses with interspecific phylogenies. Current geographical distributions of three species (a) are used to infer geographical modes of speciation. When
species that overlap geographically are sister taxa (b), sympatric speciation is inferred. When sister species do not overlap geographically (c), sympatric speciation is
rejected and allopatric speciation is inferred. When sister species do not overlap and the range of one is smaller than the range of the other (d), peripatric speciation is
inferred.
occurrence of range shifts through time: some extant
species are now found in localities in which they did not
occur prehistorically, and vice versa [32– 40]. Second,
observational studies in historical time have directly
documented countless changes in geographical distri-
butions [26,41 – 46]. Third, population genetic analyses
routinely uncover evidence for geographical range expan-
sions (e.g. [47,48]). As a result, the present-day range of a
species will often differ greatly from the range of that
species when it first arose; for this reason, several authors
have concluded that evolutionary inferences concerning
the geography of species in the past will often not be
reliable [14,41,49–51].
These concerns are magnified further when attempts
are made to reconstruct the geographical speciation mode
of ancestral taxa (e.g. [8,9,19,21,22]). Recent studies have
revealed that, under many circumstances, phylogenetic
comparative methods are unable to reconstruct ancestral
traits accurately; this is particularly true when the trait is
evolutionarily labile, such that the rate of trait evolution is
high relative to the rate of speciation [52– 54], as might be
the case for geographical range. Moreover, inferences
about the geographical distributions of ancestral taxa
deduced from the ranges of their descendants are based on
a method that does not seem very robust (K.A. Crandall,
PhD thesis, Washington University, 1993, [25]): this
method reconstructs the geographical range of an ances-
tral species as the sum of the ranges of its descendants
(Fig. 2, Box 2). These reconstructions thus not only assume
that geographical ranges of species remain constant after
Box 1. Phylogenetic reconstruction of the geographical mode of speciation
Phylogenetic approaches to the geography of speciation (e.g. [2,8,56,78])
use present-day geographical distributions and phylogenetic relation-
ships to infer the geographical context of speciation. In this approach, the
current distribution of an extant taxon is used as a character state and
comparison of the range of sister taxa enables a decision to be made
about which mode of speciation was involved. For extant sister species,
present-day distributions are compared and their size and extent of the
overlap of the ranges is used to infer geographical mode of speciation. For
example, sister species with broadly overlapping ranges would be
inferred to have originated by sympatric speciation, whereas sister
species in which the ranges were nonoverlapping and in which the range
of one taxon was relatively small (,5%) compared with the range of the
other species would be considered as evidence of peripatric speciation.
Precise criteria for distinguishing geographical modes differ among
authors. For example, Mattern and McLennan [19] consider any overlap
among the ranges of sister taxa to be indicative of sympatric speciation,
whereas Lynch [8] considers ,20% overlap to be trivial.
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Vol.18 No.5 May 2003 221
speciation, but also that entire clades do not experience
range contraction or expansion and that extinction does
not occur [2,15,55,56].
Allopatric versus sympatric speciation
Because of the unreliability of inferences of geographical
ranges in the past, interspecific phylogenetic approaches
are unlikely to add much to the debate over sympatric
versus ALLOPATRIC SPECIATION . Consider first sympatric
speciation. Can a null hypothesis that speciation was not
sympatric be rejected if sympatric species are found to be
sister taxa? Given the potential for the evolutionary
lability of geographical range, the finding that sympatric
species are sister taxa does not strongly refute the
alternative possibility that the species speciated in
allopatry or parapatry and subsequently expanded their
ranges to come into sympatry. Indeed, this is the heart of
the classic debate about sympatric speciation: proponents
note that sympatric species are closely related and infer
that sympatric speciation has occurred; detractors con-
sider sympatric speciation to be unlikely on theoretical
grounds and consider allopatric speciation followed by
range expansion to be a more probable explanation [56,57].
Thus, phylogenetic approaches to the study of putative
cases of sympatric speciation really do no more than test
the usually implicit assumption that the sympatric species
truly are sister taxa. Finding that the two species are not
sister taxa would, of course, undermine support for a
sympatric speciation scenario (e.g. [24,58,59]), but finding
that they are sister taxa would not address the primary
When one or both of the sister taxa are ancestral nodes in a
phylogeny, the geographical range of these ancestral taxa must be
inferred before sister-taxon comparisons can be made. In this case, the
ancestral taxon is assigned a geographical distribution that encom-
passes the distribution of all of its descendants [8,12,56,78]. Then, the
ranges of sister taxa are compared in the same manner as are those
ranges of extant sister species.
For the phylogenetic method to provide accurate inferences about
speciation, two related assumptions must be met. First, when compar-
ing sister species, one must assume that the current geographical
distribution correlates strongly with the geographical distribution at the
time of speciation. Second, to infer the geographical distributions of
ancestral taxa, one must assume that distributions are so static that
ancestral geographical ranges can be inferred from the ranges of their
descendants [2,8,15,56,71]. Because of the restrictive nature of this latter
assumption, even some proponents of these methods recommend
focusing on more recent divergence events (e.g. [8]).
222 Opinion TRENDS in Ecology and Evolution
TRENDS in Ecology & Evolution
Fig. 2. Geographical ranges of lions (Panthera leo), tigers (P. tigris) and jaguars
(P. onca). Mattern and McLennan [19] reconstructed speciation modes in a study
of feline evolutionary diversification and concluded that sympatric speciation was
the most common mode of speciation in cats. For example, they concluded that
the lion is the sister taxon to a clade comprising the tiger and the jaguar. The
ranges of the lion (blue) and tiger –jaguar (red) clades overlap in western Asia
(purple) and the species differ ecologically, leading to the conclusion that the split
between these two lineages occurred through sympatric speciation (historical
range of lion and tiger are based on maps from [77]). Through this sort of reason-
ing, the authors conclude that sympatric speciation accounted for 51.8% of felid
speciation events, even though they acknowledge that felines are ‘large, highly
mobile creatures’ and that the assumption that ‘postspeciation dispersal does not
overwhelm speciations patterns’ might have ‘been violated to some extent’. Note
that this is an extreme version of the phylogenetic method. Other proponents of
this method (e.g. [8]) might not consider the range overlap substantial enough for
a claim of sympatric speciation.
concerns of critics, which do not hinge on the evolutionary
relationships of the taxa.
For these reasons, interspecific phylogenetic studies by
themselves add little support to claims of sympatric
speciation (or for claims of PARAPATRIC SPECIATION , to
which the same criticisms apply). For example, vertebrates,
particularly species that tend to be highly mobile, have
always been considered to be unlikely candidates for
sympatric speciation. Hence, phylogenetically based studies
that concluded that 52% of speciation events in felids [19]
(Fig. 2) and .20% of speciation events in birds [8,14,16] were
the result of sympatric speciation were quite surprising. In
light of the potential lability of geographical range discussed
above, we suspect that we are not alone in finding these
results unconvincing (see [14] for similar conclusions from a
detailed analysis of 13 avian clades).
Box 2. The relationship between geographical modes of speciation and adaptive evolution
As a corollary to phylogenetic approaches to the geography of
speciation, several workers [12,13,16] have suggested that not only
the geographical mode of speciation, but also the underlying
process driving speciation, can be determined from examination of
phylogeny. In particular, they argue that some modes of speciation,
such as peripatric speciation, involve adaptive evolution, whereas
other modes, such as vicariant speciation, do not. However, this
assumption is unwarranted – no relationship necessarily exists
between the geographical mode of speciation and underlying
evolutionary process [79].
Although parapatric and sympatric speciation almost certainly
involve adaptive processes, vicariant speciation and peripatric specia-
tion have no necessary relationship with adaptive versus nonadaptive
evolutionary processes. For example, field and laboratory studies
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Vol.18 No.5 May 2003
This is not to say, however, that phylogenetic studies
can never be used to make a case for sympatric speciation;
combined with additional evidence that argues against a
scenario of nonsympatric speciation followed by range
expansion, phylogenetic studies can make the case for
sympatric speciation more compelling [10]. The best
documented such case involves two crater lakes in
Cameroon, each of which is occupied by its own clade of
cichlid fish [60] (Fig. 3). The most parsimonious conclusion
is that, in each crater, a single ancestral species colonized
the crater and subsequently speciated repeatedly. The
topographical and ecological homogeneity of these small
(,5 km2) craters suggests few opportunities for allopatric
speciation; indeed, it is situations such as this, in which an
allopatric phase of differentiation seems inconceivable,
that have prompted many claims of sympatric speciation
in the literature. The most plausible allopatric scenarios
would require either that ancestral populations became
geographically isolated in these tiny and apparently
homogeneous lakes (cf. [61,62]) or that each of the 20
species in the two lakes was the result of dispersal by
related species that lived outside of the lake and that
subsequently went extinct, thus rendering the lake species
monophyletic relative to other extant species. Such
scenarios are plausible, although less parsimonious than
a straightforward hypothesis of sympatric speciation.
Although phylogenetic studies have suggested surpris-
ingly high rates of sympatric speciation, allopatric specia-
tion is still usually identified as the predominant mode in
such studies [8,9,14,63]. This result is not surprising
because the taxa in most phylogenetic studies apparently
were chosen, not because they had been suggested as
potential cases of nonallopatric speciation, but rather
because data about geographical ranges and phylogenetic
relationships were available for those taxa. If allopatric
speciation is the predominant mode of speciation in most
types of animal, as most workers believe, and if study taxa
are chosen randomly with respect to likelihood of speciat-
ing in a particular manner, then one would expect to find a
predominance of cases of allopatric speciation.
However, for the same reasons discussed with regard to
sympatric speciation, finding that sister taxa are allopatric
is not definitive support for allopatric speciation; sympa-
tric speciation followed by range shifts leading to allopatry
indicate that allopatric populations are more likely to speciate when
selection causes their adaptive divergence [80 –83]. Consequently,
evidence favoring the vicariant mode of geographical speciation does
not constitute evidence that adaptation was not involved in the
speciation process; quite the contrary, these studies indicate that
vicariant speciation is more likely when adaptation is involved.
Furthermore, founder-induced or peripatric speciation does not require
that the daughter species undergo adaptive divergence [84]. For
example, Powell [85] used experimental studies to argue that founder
effects might lead to pre-mating isolation among populations of
Drosophila pseudoobscura without accompanying adaptive diver-
gence. Hence, at least in allopatric speciation, no relationship exists
between the mode of speciation and the extent of adaptive divergence
during the speciation process.
 Opinion TRENDS in Ecology and Evolution Vol.18 No.5 May 2003 223

For example, when sister taxa occur on different islands

Pungu maclareni [64,65], are separated by physical barriers (e.g. [66]), or
share a common pattern of geographical distribution with
Konia eisentrauti
other sets of sister taxa [23], then allopatric speciation
Konia dikume would seem to be the most probable interpretation.
Sarotherodon linnellii

Barombi Mbo Crater

Vicariant versus peripatric speciation
Sarotherodon caroli Several studies have extended the approach outlined
Sarotherodon steinbachi above to distinguish between different types of allopatric
speciation (e.g. [8,9,16]). In this case, it is the relative size
Myaka myaka
of the ranges of species at the time of speciation that
Sarotherodon lohbergeri distinguishes between peripatric (or PERIPHERAL ISOLATES )
and VICARIANT SPECIATION ; similarly sized ranges indicate
Stomatepia mariae
vicariant speciation, whereas asymmetric range sizes
Stomatepia pindu indicate peripatric speciation (Fig. 1). For the same
Stomatepia mongo reasons as discussed above, however, inferences about
ancestral geographical range size are unlikely to be
Sarotherodon g. gailiaeus 'Meme' accurate in many circumstances, and hence phylogenetic
Sarotherodon gailiaeus 'Ejagham'
comparative methods might provide little insight [14].
Moreover, if Chesser and Zink [14] are correct that only
Sarotherodon g. gailiaeus 'Cross'
those peripatrically derived species that rapidly expand in
Sarotherodon galilaeus sanagaensis range size are likely to survive, then this method will not
only be inaccurate, but also biased against detecting
peripatric speciation.
Tilapia sp. 'Ejagham 1' Another approach for distinguishing peripatric from
vicariant speciation was proposed recently by Chan and
Tilapia sp. 'Ejagham 2' Moore [13], who suggested that measures of tree balance
Tilapia sp. 'Ejagham 3' could be used to distinguish between the two. In a nutshell,
Chan and Moore [13] argue that vicariant speciation will
Tilapia sp. 'Ejagham 4' produce more balanced tree topologies than will peripatric
speciation because, in peripatric speciation, the processes
Tilapia snyderae/ T. bythobates
leading to speciation occur solely in the peripheral
Tilapia bakossi population. Consequently, one daughter species (the
Bermin Crater

peripheral populations) must complete the speciation

Tilapia gutturosa
process before being able to speciate again, whereas the
Tilapia imbriferna other (the main population) can speciate again immedi-
ately; thus, the latter clade will tend to accumulate more
Tilapia flava
speciation events, leading to an unbalanced phylogenetic
Tilapia bemini/ T. spongotroktis/ T. thysi topology. By contrast, in vicariant speciation, the specia-
tion process will affect both populations equally, and thus
Tilapia guineensis 'Cross' no consistent difference should exist in the time at which
Tilapia kottae
either is able to speciate again; as a result, more sym-
metrical phylogenetic topologies would be expected.
Tilapia guineensis 'Ivory Coast' However, this method assumes allopatric speciation from
the outset and cannot distinguish between allopatric,
Tilapia zillii
parapatric and sympatric speciation; similar to vicariant
speciation, parapatric and sympatric speciation should
TRENDS in Ecology & Evolution
also produce balanced tree topologies because these
speciation processes should affect both daughter species
Fig. 3. Phylogenies of cichlid species from two small African crater lakes. The
monophyly of species in each crater and the lack of obvious barriers to gene flow in the same way. Moreover, many other explanations, such
within them makes sympatric speciation the most plausible interpretation. Repro- as the evolution of characters that promote speciation,
duced, with permission, from [60]. have been put forward to explain tree imbalance [67 – 70];
thus, the existence of imbalance, even in clades in which
could produce the same present-day pattern. Indeed, fossil allopatric speciation seems to have occurred, would not
data reveal cases in which currently allopatric species necessarily be indicative of peripatric speciation.
were sympatric in the late Pleistocene [37]; moreover,
some species of plants that are likely to have arisen Patterns of character evolution
sympatrically by allopolyploidy now have allopatric Patterns of character evolution have also been suggested
distributions separated by hundreds of kilometers [10]. as a line of evidence that can support geographical
As for sympatric speciation, the inclusion of additional interpretations (e.g. [15,16,71]), but such approaches are
data can make a case for allopatric speciation compelling. fraught with assumptions and are unlikely to be generally
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224 Opinion TRENDS in Ecology and Evolution Vol.18 No.5 May 2003

Fig. 4. Plots of geographical range overlap through time. In three out of ten actual phylogenies [fairy wrens (Malurus), cranes (Gruidae) and swordtail fish (Xiphophorus)],
most comparisons among recently divergent taxa are allopatric [as indicated by the percent range overlap (x-axis) versus evolutionary age (y-axis)], a signature of allopatric
speciation with infrequent range shifts (although the swordtail fish do not show the predicted steady increase in overlap with age). However, the remaining seven groups
closely resemble the results of null models that assume frequent range shifts, conditions under which allopatric and sympatric null models are indistinguishable. The
inability to distinguish the observed patterns from those produced by the null models suggests that inferences concerning the geographical mode of speciation cannot be
made reliably. Reproduced, with permission, from [9,21].

applicable. For example, Friesen and Anderson [16]
suggest that vicariant speciation can be ruled out for
taxa that exhibit relatively high rates of character change
because such high rates are the signature of adaptive
differentiation, which is supposed to not be involved in
vicariant speciation. However, other processes can pro-
duce high rates of character change and adaptive
differentiation might play an important role in vicariant
speciation (Box 2). We suspect that no general relationship
exists between patterns of character evolution and the
geographical mode of speciation.
Shifts in range overlap through time
Several studies have used phylogenies to test geographical
modes of speciation by examining changes in geo-
graphical range size and overlap of sister taxa through
time [8 – 10,21,24] (Fig. 4). If, for example, allopatric
speciation is predominant, then recently diverged sister
taxa will tend to be geographically nonoverlapping, and
the degree of overlap is likely to increase between deeper
phylogenetic clades as a result of geographical range
shifts. Conversely, if sympatric speciation is the norm,
then recent sister taxa will be entirely overlapping, but
sister clades deeper in the tree will be more likely to have
shifted their ranges and thus overlap less. Similar
reasoning is used to distinguish peripatric from vicariant
speciation. This test is a significant advance over previous
methods because it does not require the reconstruction of
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ancestral geographical ranges. However, it is based on the
assumption that, because geographical ranges shift over
time, the geographical signal of speciation decays with age
such that the deeper one looks in a phylogeny, the less
sister taxa will exhibit a geographical pattern that
conforms to the geographical mode of speciation they
experienced.
Barraclough and Vogler [9] conducted an important test
of this approach by using simulations to assess what
patterns would be expected for a phylogeny given different
modes of speciation and different rates of geographical
range change. These models suggest that, when a
particular mode of speciation predominates in a particular
group and ranges shift stochastically following speciation,
modes of speciation can be inferred by plotting range
overlap versus evolutionary age (Fig. 4). However, these
null models also indicate that, when rates of geographical
range change are high, it will be impossible to distinguish
among different geographical modes of speciation because
range shifts will obscure the geographical pattern of
speciation for even the most recent events (Fig. 4).
In an examination of actual phylogenies, Barraclough
and Vogler [9] found that, although many sister species are
allopatric and range overlap increases with age in some
groups, suggesting allopatric speciation, this correlation is
always weak and confidence limits around the y-intercept,
which represents geographical overlap at time of specia-
tion, are often very large. Unfortunately, in most groups,
 Opinion TRENDS in Ecology and Evolution
the correlation between evolutionary age and geographical
overlap is indistinguishable from simulations that incor-
porate high rates of geographical range change, regardless
of whether the geographical mode of speciation in the
simulations is allopatric or sympatric [9,21] (Fig. 4). In
other words, the pattern frequently observed in real
phylogenies cannot be used to make inferences about the
geographical mode of speciation. Given that the true rate
of change in geographical range will usually be unknown
and, in many cases, might be large, drawing firm
conclusions from these studies will be difficult. The one
exception is groups in which almost all sister taxa are
allopatric and in which only sister taxa deep in the tree
exhibit geographical overlap [24] (Fig. 4). In such cases, a
conclusion that allopatric speciation has occurred is
reasonable, although it seems unlikely that, even in the
absence of these methods, anyone would have considered
such geographical patterns to be the result of any other
mode of speciation.
In summary, Barraclough and Vogler find that, under
the conditions of their null model, allopatric speciation and
sympatric speciation can be distinguished by plotting
range overlap versus age, but only when range shifts have
been relatively infrequent. In practice, few phylogenies
present the clear-cut pattern exhibited by the null models,
suggesting either that range shifts are too frequent to
leave a signature in most groups or that a single mode of
speciation rarely dominates in a given group.
Box 3. Historical population genetics and the geography of speciation
Coalescent approaches to population genetics have been developed
over the past 20 years to examine the historical processes responsible
for patterns of genetic variation that exist within and among
populations (reviewed in [86]). Some coalescent methods, which
have been developed primarily to test demographic, genetic and
ecological mechanisms of speciation, might also be useful for testing
geographical modes of speciation.
Several methods test the simple null hypothesis of complete isolation
of incipient species versus more complex models that involve
divergence-with-gene-flow, natural selection, or both [87 –90]. Kliman
et al. [88] applied such an approach to a study of the Drosophila
simulans complex, finding that a simple isolation model provides a
good fit to the divergence between the cosmopolitan D. simulans and
two island endemic forms, D. mauritiana and D. sechellia, suggesting
the occurrence of allopatric speciation (perhaps not a surprising result
given the geographical distribution of these species). By contrast,
Machado et al. [87] rejected the strict isolation model and found
evidence that some gene flow has occurred between D. persimilis and
D. pseudoobscura since these species began diverging, but not recently.
These methods appear to be quite promising for distinguishing
among models of isolation, divergence-with-gene-flow, and natural
selection when data from multiple independent loci are available.
However, this does not necessarily directly translate into distinguishing
among alternative geographical modes of speciation (a purpose for
which these methods were not originally intended). In the case of
D. persimilis and D. pseudoobscura, support for the divergence-with-
gene-flow model might be the result of limited gene flow throughout the
speciation process, as might be expected under sympatric or parapatric
speciation, or limited gene flow following secondary contact between
species whose initial divergence occurred in allopatry. Similarly,
selection at some loci, but not others, during species divergence
might occur in sympatry or parapatry, or might be the result of
secondary contact and reinforcement following speciation in allopatry
[89].
In some cases, additional analyses could be used to distinguish
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Vol.18 No.5 May 2003 225
The future of phylogenetics in the study of the
geography of speciation
Because speciation occurs at the population/species inter-
face, methods are needed that focus at that level [25,72].
One recent approach has been to use phylogenetic
approaches to focus solely on recent divergence events,
either between populations within a species or within
closely related species (reviewed in [73]). These
approaches propose that the phylogenetic structure of
genetic variation among populations and very recently
diverged species will differ depending on geographical
mode of speciation. For example, the finding that a small
and geographically isolated population was closely related
to a population of a geographically widespread species,
rendering that species paraphyletic, might indicate the
occurrence of recent peripatric speciation [72]. More work
is needed to validate these types of prediction, although
the more general concern still remains of whether, even
among such closely related taxa, one can assume that post-
speciation range shifts have not obscured patterns of
speciation.
Other recent approaches have moved even closer
toward the population– species interface (Box 3). These
historical population genetic methods can estimate several
parameters that might be useful in attempts to distinguish
among alternative geographical models of speciation, such
as historical population size and rates of gene flow, and
could also be used to detect the signature of some
among alternative geographical modes at a finer scale. For example, if
the data fit a model of strict isolation, estimation of historical effective
population sizes of sister species at the time of speciation might be
possible [91]. These estimates could then be used to test the hypothesis
of peripatric speciation, which predicts greatly different population sizes
in sister species at the time of speciation. Hare et al. [92] used this
approach to find that historical effective populations sizes of two
dolphin species with antitropical distributions have been very large
throughout their history, which suggests that their divergence did not
involve small peripatric populations.
Other methods, such as nested clade analysis [93], directly incorpor-
ate haplotype trees with geographical information to test whether
phylogeographical associations are due to recurrent gene flow or
historical events, such as fragmentation, colonization and range
expansion. Such analyses of the dynamical history of the geographical
range of a population might sometimes be crucial for discriminating
between alternative geographical modes of divergence [93,94]. For
example, this method has been used to show that partially overlapping
distributions of phylogenetically distinct groups could be due to
divergence in allopatry followed by range expansion [93].
Of course, all of the population-level analyses discussed above have
assumptions of their own that could limit their ability to answer
questions about the geography of speciation [87,92,95]. For example,
methods for estimating ancestral effective population sizes assume
panmixia in the ancestor and both descendants, an assumption that,
when violated, could result in rejection of the isolation model or
unrealistic estimates of historical effective population sizes [87,92].
However, historical population genetic approaches will undoubtedly
provide fresh new insights into the process of speciation, particularly
when coalescent analyses of multiple independent loci are combined
with standard phylogenetic or phylogeographical analyses. Advances
such as the ongoing application of likelihood and Markov Chain Monte
Carlo methods are likely to improve the complexity and utility of these
methods even further [87]. Whether these approaches will provide
insight into the geography of speciation remains to be seen.
226 Opinion TRENDS in Ecology and Evolution
important historical processes, such as population frag-
mentation and range shifting. These new approaches hold
17
great promise for addressing key questions concerning
speciation; whether they can resolve debate about alterna-
tive geographical modes of speciation, and avoid the
pitfalls described above, remains to be seen.
18
Conclusions
The past 15 years have seen a remarkable revolution in 19
comparative biology: phylogenetic historical perspectives
have gone from being completely ignored to being 20
ubiquitous. As with many conceptual breakthroughs,
however, the pendulum has swung too far the other way
and re-examination of the utility of these methods has 21
begun (e.g. [74 – 76]). Phylogenetic approaches, similar to
any other analytical method, have their own particular
22
assumptions. When those assumptions are met, phylo-
genetic approaches represent powerful approaches for
addressing many important questions in evolutionary 23
biology. Conversely, when they are not met, as appears
often to be the case here, then interspecific phylogenetic 24
methods generally will not be useful.
25
Acknowledgements
We thank M. Francis Benard, L. Harmon, J. Kolbe, J. Wakeley,
D. Ziolkowski and three anonymous reviewers for comments. Peter 26
Jackson shared his expertise on the geographical range of wild felids. This 27
work was supported by the National Science Foundation (DEB 9982736).
28
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